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John R. Bach, MD Carlo Bianchi, MD Mauro Vidigal-Lopes, MD Sandra Turi, MD Giorgio Felisari, MD


From the Department of Physical Medicine and Rehabilitation, University of Medicine and Dentistry of New Jersey–New Jersey Medical School, Newark, New Jersey (JRB); Divisione di Riabilitazione, Fondazione Istituto Sacra Famiglia, Cesano Boscone, Milan, Italy (CB, ST, GF); and Vent-Lar Muscular Dystrophy Program–Julia Kubitschek Hospital and the Servic ¸ o de Pneumologia e Cirurgia Tora ´ cica of the Madre Teresa Hospital, Belo Horizonte, Minas Gerais, Brazil (MV-L).


Lung Inflation by Glossopharyngeal Breathing and “Air Stacking” in Duchenne Muscular Dystrophy
Bach JR, Bianchi C, Vidigal-Lopes M, Turi S, Felisari G: Lung inflation by glossopharyngeal breathing and “air stacking” in Duchenne muscular dystrophy. Am J Phys Med Rehabil 2007;86:295–300.

All correspondence and requests for reprints should be address to John R. Bach, MD, Professor of Physical Medicine and Rehabilitation, Professor of Neurosciences, Vice Chairman, Department of Physical Medicine and Rehabilitation, University Hospital B-403, 150 Bergen St., Newark, NJ 07103. 0894-9115/07/8604-0295/0 American Journal of Physical Medicine & Rehabilitation Copyright © 2007 by Lippincott Williams & Wilkins
DOI: 10.1097/PHM.0b013e318038d1ce

Objective: To compare the use of glossopharyngeal breathing (GPB) and air stacking to increase lung volumes and cough peak flows (CPF), and GPB to increase ventilator-free breathing ability (VFBA), for patients with Duchenne muscular dystrophy. Design: A case series of all referred patients with declining vital capacity (VC). Seventy-eight patients underwent training in and monitoring of the efficacy of air stacking (retaining consecutively delivered volumes of air delivered via manual resuscitator and held by glottic closure) to maximum insufflation capacity (MIC). GPB also was demonstrated to all 78 patients, and 32 were formally trained and prescribed GPB as their VCs decreased below 400 ml. To be successful, the MIC or GPB maximum single-breath capacity (GPmaxSBC) had to exceed VC. Improvements in VFBA were determined by requiring fewer ventilator-assisted breaths per minute. CPFs were measured by peak flow meter. Results: Seventy-four (94.9%) of the patients could air stack (MIC Ͼ VC), and, thus far, 21 (27%) are able to GPB. Fifteen could GPB sufficiently to delay onset of daytime ventilator use and, later, to require 1.9 fewer ventilator assisted breaths per minute. For the 47 patients with multiple data points, as VC deteriorated from 1080 Ϯ 870 to 1001 Ϯ 785 ml, MIC increased from 1592 Ϯ 887 to 1838 Ϯ 774 ml. For 21 patients, GPmaxSBC significantly exceeded VC (824 Ϯ 584 vs. 244 Ϯ 151 ml, respectively, P Ͻ 0.001). The ability to increase lung volume by air stacking (MIC) was better retained than was the ability to increase lung volume by GPB (GPmaxSBC). Air stacking also permitted assisted CPF to exceed unassisted CPF: 289 Ϯ 91 and 164 Ϯ 76 liters/m, respectively (P Ͻ 0.001). Conclusions: GPB and air stacking can increase lung volumes and, thereby, cough flows. GPB also can be used in many cases to delay and decrease daytime ventilator use.
Key Words: Glossopharyngeal Breathing, Cough, Duchenne Muscular Dystrophy, Respiratory Therapy, Noninvasive Mechanical Ventilation, Life Expectancy

April 2007

Lung Inflation by Glossopharyngeal Breathing


cessation of ventilator use results in immediate distress and blood-gas deterioration. Two methods of lunginflation therapy that can result in increased cough flows are air stacking and maximum-depth glossopharyngeal breathing (GPB). Phys. Air stacking was performed by the patient receiving consecutively delivered volumes of air from a manual resuscitator or a volume-cycled ventilator via a mouthpiece. VC plateaus at age 19. we prospectively determined whether the ability to air stack and GPB could improve with practice and result in improved VFBA and cough flows.13 Indeed. Even then. and air stacking was easier to master and the ability easier to retain over time for deep lung expansion. Four of the 78 patients had taken glucocorticoids. and each patient was screened for the ability to exceed VC by GPB.15 If initially unsuccessful. Training was facilitated by monitoring gulp efficiency.1. All 74 self-directed patients mastered air stacking when initially introduced to it (MIC Ͼ VC) and were asked to practice it two to three times per day. enzymatic.1 This makes air stacking and GPB increasingly important for the autonomous augmentation of cough flows. electromyographic. T MATERIALS AND METHODS This work was approved by the hospital ethics committee. and then blow the volume into a spirometer. Thus.10.7 Subsequently. The age and magnitude of the plateau was documented by pre.8 This contributes to the decrease in unassisted CPF.he key to the successful long-term use of noninvasive mechanical ventilatory support is in effectively expelling airway secretions when necessary. 86. Once a patient demonstrated mastery (maximum single-breath capacity [GPmaxSBC] ϾVC). GPB was taught by having the patient take a deep breath and hold it. Advances made during the last two decades in noninvasive mechanical ventilatory support and mechanically assisted coughing have greatly improved survival without resort to tracheotomy.1 The VFBA is considered limited when patients need intermittent positive pressure ventilations to supplement unassisted minute ventilation to prevent distress and to maintain baseline blood-gas levels.and post-VC measurements below a maximum (plateau) for 24 patients. DMD patients who are not taught and equipped with respiratory muscle aids to avoid respiratory failure often undergo tracheotomy before they are able to benefit from GPB for ventilator-free breathing ability (VFBA).14 GPB practice was considered optional before this point because it could not be used for VFBA early on. which was defined as (GPmaxSBC Ϫ VC) Ϭ (number of gulps to a maximum insufflation) in milliliters per gulp. Dail first described GPB as gulping air into the lungs for the purpose of providing deep lung volumes to increase the cough flows of five postpoliomyelitis patients. a demonstration videotape was dispensed. Med. The initial appointment for 16 patients had been before 1996. The GPmaxSBC was the maximum volume that could be gulped in.3– 6 In 1981. J. Each patient was asked about his practice efforts at every visit. voice volume. it was reported that 47 Duchenne muscular dystrophy (DMD) patients reached a maximum (plateau) vital capacity (VC) between ages 10 and 12 (range 9 –16). GPB was demonstrated after VC plateau at every clinic visit. 10 –15 maneuvers each time. If he had not mastered GPB by the time his VC had decreased to 400 ml (the point at which many patients with DMD begin to use daytime ventilatory assistance). Air stacking involves the use of a manual resuscitator or volume-cycle ventilator to deliver volumes of air that are consecutively held by glottic closure until no more air can be retained. Gene-deletion studies were positive for 54 of 70 patients. or oral–nasal interface and retaining as much as possible with a closed glottis (MIC).11 Use of GPB for ventilator-free breathing has been reported for high-level traumatic tetraplegia patients and poliomyelitis patients. he was asked to practice it three times a day. as typified by the patient record in Figure 1. Rehabil. and VFBA. nasal. GPB mastery also can eliminate fear of ventilator dysfunction or disconnection. All patients were trained in air stacking and were given a demonstration of GPB after the plateauing of the VC.11–13 but not for DMD patients.2 To do so. the patient’s nostrils were sealed to demonstrate to him the need for the soft palate to seal off the nasopharynx.9 The volume was then measured spirometrically to determine MIC. No. or it was assumed for the others because of their age and because subsequent data points were lower than the initial VC measurement. Thirty-one of 47 who returned for at least one follow-up visit reported performing it at least twice daily. from then on. nine patients could not master the glottic movements necessary for successful GPB. Vol. VC decreases by 5–10% per year in patients with DMD. All except one lost the ability to walk by age 11.9 The maximum lung volume that can be held by air stacking is the maximum insufflation capacity (MIC). When absent. 4 . Seventy-eight consecutive males who had visited a clinic since 1996 were studied after VC plateau.7. then imitate the clinician and take 15–20 gulps. in the general population. ● 296 Bach et al. and GPB practice was formally prescribed. the augmentation of lung air volumes can be crucial to optimize cough peak flows (CPF). On obserAm. and biopsy assessments. The diagnosis was based on clinical.

For these 31. respectively. VC. Two patients lost the ability to air stack (MIC ϭ VC) at ages 26 and 38. Eighteen of the 19 reported using GPB daily. Ten patients had mastered GPB on their own and presented with GPmaxSBC ϾVC. and CPF changes over time for the 47 patients with multiple data points during a 7. and most recent evaluations were made by t test using the Bonferroni correction for six comparisons.FIGURE 1 Graphic for a patient with 20 data points. Diminished VFBA was defined by lack of autonomous ability to breathe without using 169-mo follow-up are illustrated in Figure 2. April 2007 297 . nor did they have the glottic closure gulp (click) that is heard with successful GPB. MIC plateaued at 21 Ϯ 18 (2–51) mos after initial training. Twenty-two others were formally taught GPB. Twenty-four DMD patients’ VCs plateaued at mean age 12.1 (range 10. to the extent that only resumption of GPB or deep. and CPF. Patients took these assisted breaths to avoid dyspnea. glossopharyngeal maximum single-breath capacity.6 Ϯ 3. For 31 of the 47 patients who reported practicing air stacking at least twice a day. vital capacity. they did not have as much rostral– caudal movement of the glottis as did patients whose GPmaxSBC exceeded VC.1) yrs. GPmaxSBC. and the most recent data. Unassisted and assisted CPF were measured by Access Peak Flow Meter (Health Scan Products Inc. NJ) at every visit. For 11 of the 19. A standard oral–nasal mask was used for spirometry and CPF measurements. or by a difference in need for mouthpiece intermittent positive-pressure ventilations during 5-min periods when using GPB vs. and GPmaxSBC. Their mean initial VC. Delayed onset of daytime ventilatory assistance was recognized when patients who normally used GPB throughout waking hours became dyspneic and hypercapnic when breathing without it. London. plateau. Assisted CPF are defined as CPF augmented by an abdominal thrust that is timed to glottic opening after air stacking or GPB to deep lung inflation. The maximum of four or five measurements was recorded for the initial (post-VC plateau) VC. at 2026 Ϯ 555 (940 –2510) ml. MIC. MIC. GPmaxSBC increased with practice and plateaued 13 Ϯ 16 (range 3– 49) mos after initial mastery Lung Inflation by Glossopharyngeal Breathing Statistical Analysis Descriptive statistics included mean and standard deviations. and GPmaxSBC were measured spirometrically (Mark 14 spirometer. respectively. vation. The VC.1 yrs) were taught air stacking after their VC was on the decline. VC. and unassisted and assisted CPF were 145 Ϯ 112 and 250 Ϯ 84 liters/m. Cedar Grove. Ltd. Eight of the 47 patients’ postplateau VCs increased by 35–70 ml for one or more follow-up visits after practicing lung-insufflation therapy.5–16. the maximum observed assisted CPF. GPmaxSBC. This warranted a P value Ͻ0. Ferraris Development and Engineering Co. ventilator-assisted breaths could maintain them. MIC. MIC. UK). but four were too cognitively impaired to learn lung-inflation techniques. periods when it was not used. The 74 remaining self-directed patients (mean age 20. The VC and GPmaxSBC changes over time for 19 of the 32 patients who mastered GPB and had two or more data points are illustrated in Figure 3. maximum insufflation capacity. were 987 Ϯ 631 and 1501 Ϯ 618 ml. and MIC by air stacking.008 for statistical significance. MIC. with no change in end-tidal carbon dioxide or oxyhemoglobin saturation.7 Ϯ 3. the MIC increased over time despite diminishing VC. Comparisons between mean values of MIC and GPmaxSBC with VC at the initial. RESULTS All 78 patients cooperated for VC measurements.

FIGURE 4 Changes in vital capacity (VC) and glossopharyngeal breathing. and at least nine are likely to never master it.5 (13.5) yrs. Age at initial GPB mastery 24. Gulp capacities were from 8 Ϯ 9 to 70 Ϯ 34 ml.8 Ϯ 4.008). Maximum single-breath capacity (GPmaxSBC) for 11 patients whose GPmaxSBC increased over time.3 (17.5) yrs.2) yrs. and unassisted and assisted cough peak flows (CPF) over time for 47 patients with two or more data points.5–33.1–31.0) yrs. depending on whether GPB was being used for normal minute ventilation or for maximal lung inflation. All used volume-cycled ventilators on assist/control mode with delivered volumes of 850 –1500 ml and a backup rate of 10 –12 per minute. The mean age of beginning nocturnal noninvasive ventilation was 19.1) yrs. and two had GPmaxSBC exceed VC by 80 and 240 ml at initial mastery but have not yet returned. with the latter gulps being much smaller. most recent evaluation 29. Some of the remaining 42 may master it as their VCs decrease below 400 ml.FIGURE 2 Changes in vital capacity (VC).4 Ϯ 1.6 (24. Fifteen patients eventually used GPB throughout daytime hours such that respiratory distress and hypercapnia developed when ceasing GPB.8 (18 –33.7 (23. No. GPB delayed the need for daytime ventilator use. GPmaxSBC can exceed VC.6 –37.1 Ϯ 3.3 (17.3 yrs.3 Ϯ 1. age initially 20. (Figure 4). and for the patients in Figures 2– 4. ● Vol. including eight whose GPmaxSBC did not increase with training.3 (17.5 (13.7 mouthpiece intermittent positivepressure ventilations per minute (1200 ml each) when not using GPB and 3. Thus. maximum GPmaxSBC 25. at maximum 21. For the 74 patients as a whole.1–33) yrs. Although all of our GPB users lost the ability to breathe unaided by ventilator use. only 21 of 78 (26. most recently 24. Phys. Six patients died during the course of the study: FIGURE 3 Changes in vital capacity (VC) and glossopharyngeal breathing maximum singlebreath capacity (GPmaxSBC) over time for 18 patients.9 Ϯ 4. the MIC and GPmaxSBC values significantly exceeded VC and assisted CPF exceeded unassisted CPF (P Ͻ 0.7– 43.2 Ϯ 5.5– 31. Nine of the 32 patients did not master GPB. Thus. these 15 required 5.2– 43.1) yrs of age.6 Ϯ 4.9%) have mastered GPB thus far.7 ventilations per minute when using it.4 Ϯ 4. it can delay the need for daytime ventilator use.3 Ϯ 5. At the most recent evaluation. Rehabil. 86.4 Ϯ 4. Med.1) yrs of age. for at least 27% of DMD patients. Whereas 74 of 78 (95%) patients with DMD mastered air stacking. 4 .9 Ϯ 4. and for most of these. maximum insufflation capacity (MIC).1 (13. Age at initial GPB mastery 24. at most recent evaluation 30. 298 Bach et al. J. none have tracheostomy tubes. Am. at GPmaxSBC maximum 27.1 Ϯ 4.1) yrs.9 – 43.

9 it is important for patients to be able to autonomously increase lung volumes when they need to cough. as assisted CPF and air-stacking ability decrease.24 Lung packing by GPB is used by many breath-hold divers to increase lung air volumes by up to 5. despite some being over age 40. subsequently. temporary increase in VC for eight patients was probably attributable to an improvement in pulmonary compliance brought about by regular lung-expansion therapy. and GPB and cough become physically impossible for them. and many hours of VFBA despite having little or no VC. GPmaxSBCs over 3000 ml. Whereas most patients with bulbar amyotrophic lateral sclerosis lose the ability to air stack. Thus. but the lips and buccal muscles are too weak to permit air delivery past the vocal fold. and by many competitive swimmers to increase thoracic volumes and buoyancy. both should be monitored regularly. and practice should be encouraged. who often have gulp capacities over 100 ml. DISCUSSION The VC plateau that we found for 24 patients occurred months later than the figure reported previously. although DMD patients are usually able to speak clearly.13 This is because bulbarinnervated muscles tend to be spared for the latter but become increasingly dysfunctional in DMD. and maintain good vocal-fold mobility and glottic closure even April 2007 after 40 yrs of age.7 The fact that 4 of our 24 patients received glucocorticoid therapy may be one of the reasons for this. Some patients can only GPB or air stack with the nose plugged because the soft palate is unable to seal off the nasopharynx. deep lung insufflations and abdominal thrusts have been separately shown to increase CPF almost equally. When air stacking and GPB are suboptimal. as for these DMD patients. or by using the CoughAssist machine (J. Some patients learn it on their own.five from overt cardiac failure. This is probably a consequence of cerebral imprinting of the phylogenetic distribution of lung-ventilation mechanisms. with the greatest increases when they are combined. when MIC is greater than GPmaxSBC. from respiratory failure during a respiratory tract infection. take food by mouth.1 they lose the ability to close the glottis tightly enough to hold deep lung volumes. by delivering high volumes from a volume-cycled ventilator.5. the hypopharyngeal musculature is weakened and laryngeal mobility is impaired. Also.18 GPB. It is possible that the mechanism for GPB is the same as that observed in experimental studies in lunged amphibians for whom buccal pumping activity increases during hypoxia and hypercapnia.21 few clinicians are familiar with the technique. Cambridge.12. and GPB saved them some effort in having to rotate the neck and grab the mouthpiece as much as would have been necessary otherwise. MA) at insufflation pressures of 40 cm H2O or more via an oronasal interface. Emerson Company. Lung-inflation therapy also helps maintain both dynamic and static pulmonary compliance.16 The delayed need to use daytime ventilatory support and.12.22 Indeed. it was reported that three DMD patients used GPB to inflate the lungs to two to three times VC. Some such patients can air stack better via nasal interfaces. permits this. H. lung-insufflation therapy can still be performed using a manual resuscitator with the expiratory valve blocked. ceased GPB shortly after aspiration breathing had evolved. the fewer assisted breaths required when using GPB than when not using it. because 90% of episodes of respiratory failure and death for conventionally managed DMD patients occur as a result of ineffective coughing during intercurrent upper–respiratory tract infections.9. Indeed. In a previous study. Although we and others strongly recommend that GPB be taught to patients with neuromuscular disorders.22–27 The transpulmonary pressures generated by maximal-depth GPB in swimLung Inflation by Glossopharyngeal Breathing 299 . The authors did not report any effect on cough flows or on VFBA.13 The GPmaxSBCs and gulp volumes in DMD patients tend to be lower than those reported for postpolio and spinal cord–injured patients.17 and because cough flows correlate with (pre-) cough volumes. Likewise. and one.23. like air stacking via a volume ventilator. Aspiration breathers. Pressure-cycled ventilators such as BiPAP machines do not permit air stacking and should not be used for these patients. then the glottis is sufficiently intact to hold deep lung volumes. Although we only measured the effect of deeper lung volumes and abdominal thrusts on assisted coughing.6 liters over VC to permit longer submersion. Because both GPmaxSBC and MIC can improve and plateau over a wide range of time (2–51 mos) despite declining VC. When the GPmaxSBC is greater than the MIC achieved by air stacking via a mouthpiece (as often occurs in postpoliomyelitis patients). who had no assistance at home. our patients use CoughAssist machines for both mechanically assisted coughing and for maximal lung insufflations. like mammals.20 Comparing GPmaxSBC and MIC permits the evaluation of oropharyngeal muscle groups.19 we have observed losses of air-stacking ability in only 2 of 74 DMD patients. provided some security to the patients because they could survive longer by using GPB in the event of ventilator failure. No complications have been associated with this therapy for the Ͼ1000 patients with neuromuscular diagnoses who have been treated in this manner in the last 28 yrs. The slight. at least four of our patients who learned it on their own and used it spontaneously were hypercapnic and hypoxic.

51:1121–7 Soudon P. Hall FG: Pressure-volume characterisics of “lung packing. GPB provides a vital advantage for those who master it. Shade D. Kokyu To Junkan 2003. Philadelphia.8:580–4 4. Jankowski LW. 27. PA.75:15–25 11. Kritharides L. Am J Phys Med Rehabil 1998.4:11–28 Vann RD. pp 80–3 Brainerd EL: New perspectives on the evolution of lung ventilation mechanisms in vertebrates. Proc Am Thorac Soc 2006 Ishikawa Y. 86. many DMD patients can exceed their VCs three. O’Donnell CR.5. 24. 98:613–19 Webber B. and DMD patients can use GPB instead of a ventilator for ventilatory support when awake. 19. Gustafsson P. Lee M: Long-term rehabilitation in advanced stage of childhood onset.79:222–7 10. Dail CW. it seems that this is rarely even attempted.21(suppl):42 Lindholm P. because “it cannot be mastered by all patients. It should no longer be ignored for patients with DMD.29 These are similar to the pressures we use for maximum-depth air stacking. 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